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Russian-olive (Elaeagnus angustifolia) genetic diversity in the western United States and implications for biological control

Published online by Cambridge University Press:  17 April 2019

John F. Gaskin*
Affiliation:
Research Biologist, USDA–Agricultural Research Service, Sidney, MT, USA
Jose A. Andrés
Affiliation:
Senior Research Associate, Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA
Steven M. Bogdanowicz
Affiliation:
Research Support Specialist, Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA
Kimberly R. Guilbault
Affiliation:
Graduate Student, Colorado State University, Fort Collins, CO, USA
Ruth A. Hufbauer
Affiliation:
Professor, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA
Urs Schaffner
Affiliation:
Head Ecosystems Management, Research Scientist, CABI, Delémont, Switzerland
Philip Weyl
Affiliation:
Research Scientist, CABI, Delémont, Switzerland
Livy Williams III
Affiliation:
Research Entomologist, USDA–Agricultural Research Service, Charleston, SC, USA; and European Biological Control Laboratory, Montpellier, France
*
Author for correspondence: John F. Gaskin, USDA–Agricultural Research Service, Sidney, MT 59270. (Email: [email protected])

Abstract

Invasions can be genetically diverse, and that diversity may have implications for invasion management in terms of resistance or tolerance to control methods. We analyzed the population genetics of Russian-olive (Elaeagnus angustifolia L.), an ecologically important and common invasive tree found in many western U.S. riparian areas. We found three cpDNA haplotypes and, using 11 microsatellite loci, identified three genetic clusters in the 460 plants from 46 populations in the western United States. We found high levels of polymorphism in the microsatellites (5 to 15 alleles per locus; 106 alleles total). Our native-range sampling was limited, and we did not find a genetic match for the most common cpDNA invasive haplotype or a strong confirmation of origin for the most common microsatellite genetic cluster. We did not find geographic population structure (isolation by distance) across the U.S. invasion, but we did identify invasive populations that had the most diversity, and we suggest these as choices for initial biological control–release monitoring. Accessions from each genetic cluster, which coarsely represent the range of genetic diversity found in the invasion, are now included in potential classical biological control agent efficacy testing.

Type
Research Article
Copyright
© Weed Science Society of America, 2019 

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Footnotes

Associate Editor: Marie Jasieniuk, University of California, Davis

References

Asadiar, LS, Rahmani, F, Siami, A (2013) Assessment of genetic diversity in the Russian olive (Elaeagnus angustifolia) based on ISSR genetic markers. Rev Ciência Agron 44:310316 CrossRefGoogle Scholar
Bateman, HL, Paxton, EH, Shafroth, PB (2009) Saltcedar and Russian olive interactions with wildlife. Pages 143 In Shafroth, PB, Brown, CA, Merritt, DM, eds. Saltcedar and Russian Olive Control Demonstration Act Science Assessment Reston, VA: United States Geological Survey, Scientific Investigations Report 2009–5247Google Scholar
Bock, DG, Caseys, C, Cousens, RD, Hahn, MA, Heredia, SM, Hübner, S, Turner, KG, Whitney, KD, Rieseberg, LH (2015) What we still don’t know about invasion genetics. Mol Ecol 24:22772297 CrossRefGoogle ScholarPubMed
Borell, AE (1971) Russian-Olive for Wildlife and Other Conservation Uses. Leaflet 292. Washington, DC: U.S. Department of Agriculture. 8 pGoogle Scholar
Bovey, RW (1965) Control of Russian olive by aerial application of herbicides. J Range Manage 18:194195 CrossRefGoogle Scholar
Burdon, JJ, Groves, RH, Cullen, JM (1981) The impact of biological control on the distribution and abundance of Chondrilla juncea in south-eastern Australia. J Appl Ecol 18:957966 CrossRefGoogle Scholar
CABI (2018) Invasive Species Compendium. https://www.cabi.org/isc/datasheet/20717. Accessed: June18, 2018Google Scholar
Carlsson, J (2008) Effects of microsatellite null alleles on assignment testing. J Hered 99:616623 Google ScholarPubMed
Christensen, EM (1963) Naturalization of Russian olive (Elaeagnus angustifolia L.). Utah. Am Midl Nat 70:133137 CrossRefGoogle Scholar
Chowdhury, MA, Jana, S, Schroeder, WR (2000) Phenotypic diversity in four woody species on the Canadian prairies. Can J Plant Sci 80:137142 CrossRefGoogle Scholar
Collette, LK, Pither, J (2015) Russian-olive (Elaeagnus angustifolia) biology and ecology and its potential to invade northern North American riparian ecosystems. Invasive Plant Sci Manag 8:114 CrossRefGoogle Scholar
DeCant, JP (2008) Russian olive, Elaeagnus angustifolia, alters patterns in soil nitrogen pools along the Rio Grande River, New Mexico, USA. Wetlands 28:896904 CrossRefGoogle Scholar
Earl, DA (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359361 CrossRefGoogle Scholar
Edwards, RJ, Clark, LC, Beck, KG (2014) Russian olive (Elaeagnus angustifolia) dispersal by European starlings (Sturnus vulgaris). Invasive Plant Sci Manag 7:425–31CrossRefGoogle Scholar
Evanno, G, Regnaut, S, Goudet, J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:26112620 CrossRefGoogle ScholarPubMed
Falush, D, Stephens, M, Pritchard, JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:15671587 Google ScholarPubMed
Falush, D, Stephens, M, Pritchard, JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574578 CrossRefGoogle ScholarPubMed
Friedman, JM, Auble, GT, Shafroth, PB, Scott, ML, Merigliano, MF, Freehling, MD, Griffin, ER (2005) Dominance of non-native riparian trees in western USA. Biol Invasions 7:747751 CrossRefGoogle Scholar
Gaskin, JF, Bon, MC, Cock, MJ, Cristofaro, M, De Biase, A, De Clerck-Floate, R, Ellison, CA, Hinz, HL, Hufbauer, RA, Julien, MH, Sforza, R (2011) Applying molecular-based approaches to classical biological control of weeds. Biol Control 58:121 CrossRefGoogle Scholar
Gaskin, JF, Hufbauer, RA, Bogdanowicz, SM (2013a) Microsatellite markers for Russian olive (Elaeagnus angustifolia; Elaeagnaceae). Appl Plant Sci 1:130001 3 CrossRefGoogle Scholar
Gaskin, JF, Schwarzländer, M, Kinter, CL, Smith, JF, Novak, SJ (2013b) Propagule pressure, genetic structure, and geographic origins of Chondrilla juncea (Asteraceae): an apomictic invader on three continents. Am J Bot 100:18711882 CrossRefGoogle ScholarPubMed
Gaskin, JF, Wilson, LM (2007) Phylogenetic relationships among native and naturalized Hieracium (Asteraceae) in Canada and the United States based on plastid DNA sequences. Syst Bot 32:478–85CrossRefGoogle Scholar
Goolsby, JA, De Barro, PJ, Makinson, JR, Pemberton, RW, Hartley, DM, Frohlich, DR (2006) Matching the origin of an invasive weed for selection of a herbivore haplotype for a biological control programme. Mol Ecol 15:287297 CrossRefGoogle ScholarPubMed
Grevstad, F, Shaw, R, Bourchier, R, Sanguankeo, P, Cortat, G, Reardon, RC (2013) Efficacy and host specificity compared between two populations of the psyllid Aphalara itadori, candidates for biological control of invasive knotweeds in North America. Biol Control 65:5362 CrossRefGoogle Scholar
Hamrick, JL, Godt, MJW, Sherman-Broyles, SL (1992) Factors influencing levels of genetic diversity in woody plant species. Pages 95124 in Adams, WT, Strauss, SH, Copes, DL, Griffin, AR, eds. Population Genetics of Forest Trees. Springer, Dordrecht, Netherlands CrossRefGoogle Scholar
Hillis, DM, Moritz, C, Mable, BK (1996) Molecular Systematics. 2nd ed. Sunderland, MA: Sinauer. 655 pGoogle Scholar
Hufbauer, RA, Roderick, GK (2005) Microevolution in biological control: mechanisms, patterns and processes. Biol Control 35:227239 CrossRefGoogle Scholar
Jasieniuk, M, Brûlé-Babel, AL, Morrison, IN (1996) The evolution and genetics of herbicide resistance in weeds. Weed Sci 44:176193 CrossRefGoogle Scholar
Jombart, T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:14031405 CrossRefGoogle Scholar
Kalinowski, ST, Taper, ML, Marshall, TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:10991106 CrossRefGoogle ScholarPubMed
Katz, GL, Shafroth, PB (2003) Biology, ecology and management of Elaeagnus angustifolia L. (Russian olive) in western North America. Wetlands 23:763777 CrossRefGoogle Scholar
Kindschy, RR (1998) European starlings disseminate viable Russian-olive seeds. Northwestern Naturalist 79:119120 CrossRefGoogle Scholar
Lesica, P, Miles, S (1999) Russian olive invasion into cottonwood forests along a regulated river in north-central Montana. Can J Bot 77:10771083 Google Scholar
Lesica, P, Miles, S (2004) Beavers indirectly enhance the growth of Russian olive and tamarisk along eastern Montana rivers. West N Am Naturalist 64:93100 Google Scholar
Little, EL (1961) Sixty Trees from Foreign Lands. Washington, DC: USDA Agriculture Handbook No. 212. 30 pGoogle Scholar
Lym, RG, Nissen, SJ, Rowe, ML, Lee, DJ, Masters, RA (1996) Leafy spurge (Euphorbia esula) genotype affects gall midge (Spurgia esulae) establishment. Weed Sci 44:629633 CrossRefGoogle Scholar
Lym, RG, Carlson, RB (2002) Effect of leafy spurge (Euphorbia esula) genotype on feeding damage and reproduction of Aphthona spp.: implications for biological weed control. Biol Control 23:127133 CrossRefGoogle Scholar
McCarthy, C, Pella, T, Link, G, Rumble, MA (1997) Greater prairie chicken nesting habitat, Sheyenne National Grassland, North Dakota. Pages 1318 in Uresk, DW, Schenbeck, GL, O’Rourke, JT, eds. Conserving Biodiversity on Native Rangelands: Symposium Proceedings: August 17, 1995. Fort Collins, CO: US Department of Agriculture Google Scholar
Mineau, MM, Baxter, CV, Marcarelli, AM (2011) A non-native riparian tree (Elaeagnus angustifolia) changes nutrient dynamics in streams. Ecosystems 14:353365 CrossRefGoogle Scholar
Müller-Schärer, H, Schaffner, U, Steinger, T (2004) Evolution in invasive plants: implications for biological control. Trends Ecol Evol 19:417422 CrossRefGoogle ScholarPubMed
Olson, TE, Knopf, FL (1986) Naturalization of Russian-olive in the western United States. West J Appl For 1:6569 Google Scholar
Peakall, R, Smouse, PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:25372539 CrossRefGoogle ScholarPubMed
Pritchard, JK, Stephens, M, Donnelly, P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945959 Google ScholarPubMed
Pritchard, JK, Wen, X, Falush, D (2007) Documentation for structure Software: Version 2.2. https://web.stanford.edu/group/pritchardlab/software/structure22/readme.pdf. Accessed: June 20, 2018Google Scholar
Protopopova, VV, Shevera, MV, Melnik, RP (2006) The history of introduction and present distribution of Elaeagnus angustifolia L. in the Black Sea region of Ukraine. Chornomorsky Bot J 2:513 CrossRefGoogle Scholar
Raymond, M, Rousset, F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248249 CrossRefGoogle Scholar
Rohlf, FJ (2009) NTSYSpc: Numerical Taxonomy System v. 2.21c. Setauket, NY: Exeter Software Google Scholar
Roman, J, Darling, JA (2007) Paradox lost: Genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454464 CrossRefGoogle ScholarPubMed
Rousset, F (2008) GENEPOP’007: a complete reimplementation of the GENEPOP software for Windows and Linux. Mol Ecol Res 8:103106 CrossRefGoogle Scholar
Taberlet, P, Geilly, L, Pautou, G, Bouvet, J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17:11051109 CrossRefGoogle ScholarPubMed
Tamura, K, Dudley, J, Nei, M, Kumar, S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:15961599 CrossRefGoogle ScholarPubMed
Tropicos (2018) Home page. http://www.tropicos.org. Accessed June 18, 2018Google Scholar
Wang, Q, Ruan, X, Huang, JH, Xu, NY, Yan, QC (2006) Intra-specific genetic relationship analyses of Elaeagnus angustifolia based on RP-HPLC biochemical markers. J Zhejiang Univ-Sci B 7:272278 CrossRefGoogle ScholarPubMed
Ward, SM, Gaskin, JF, Wilson, LM (2008) Ecological genetics of plant invasion: What do we know? Invasive Plant Sci Manag 1:98109 CrossRefGoogle Scholar
Williams, WI, Friedman, JM, Gaskin, JF, Norton, AP (2014) Hybridization of an invasive shrub affects tolerance and resistance to defoliation by a biological control agent. Evol Appl 7:381393 CrossRefGoogle ScholarPubMed
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